Emergence and Modular Evolution of a Novel Motility Machinery in Bacteria

English version České info

Bacteria glide across solid surfaces by mechanisms that have remained largely mysterious despite decades of research. In the deltaproteobacterium Myxococcus xanthus, this locomotion allows the formation stress-resistant fruiting bodies where sporulation takes place. However, despite the large number of genes identified as important for gliding, no specific machinery has been identified so far, hampering in-depth investigations. Based on the premise that components of the gliding machinery must have co-evolved and encode both envelope-spanning proteins and a molecular motor, we re-annotated known gliding motility genes and examined their taxonomic distribution, genomic localization, and phylogeny. We successfully delineated three functionally related genetic clusters, which we proved experimentally carry genes encoding the basal gliding machinery in M. xanthus, using genetic and localization techniques. For the first time, this study identifies structural gliding motility genes in the Myxobacteria and opens new perspectives to study the motility mechanism. Furthermore, phylogenomics provide insight into how this machinery emerged from an ancestral conserved core of genes of unknown function that evolved to gliding by the recruitment of functional modules in Myxococcales. Surprisingly, this motility machinery appears to be highly related to a sporulation system, underscoring unsuspected common mechanisms in these apparently distinct morphogenic phenomena.

Vyšlo v časopise: Emergence and Modular Evolution of a Novel Motility Machinery in Bacteria. PLoS Genet 7(9): e32767. doi:10.1371/journal.pgen.1002268
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002268

Souhrn

Zdroje

1. RegoATFronzesRWaksmanG 2010 SnapShot: Bacterial Appendages I. Cell 140 162 162.e1 doi:10.1016/j.cell.2009.12.047

2. RegoATFronzesRWaksmanG 2010 SnapShot: Bacterial appendages II. Cell 140 294 294.e1 doi:10.1016/j.cell.2010.01.006

3. ErhardtMNambaKHughesKT 2010 Bacterial nanomachines: the flagellum and type III injectisome. Cold Spring Harb Perspect Biol 2 a000299 doi:10.1101/cshperspect.a000299

4. PallenMJMatzkeNJ 2006 From The Origin of Species to the origin of bacterial flagella. Nat. Rev. Microbiol 4 784 790 doi:10.1038/nrmicro1493

5. MerzAJSoMSheetzMP 2000 Pilus retraction powers bacterial twitching motility. Nature 407 98 102 doi:10.1038/35024105

6. SkerkerJMPrasolMSPerchukBSBiondiEGLaubMT 2005 Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol 3 e334 doi:10.1371/journal.pbio.0030334

7. PelicicV 2008 Type IV pili: e pluribus unum? Mol. Microbiol 68 827 837 doi:10.1111/j.1365-2958.2008.06197.x

8. JarrellKFMcBrideMJ 2008 The surprisingly diverse ways that prokaryotes move. Nat. Rev. Microbiol 6 466 476 doi:10.1038/nrmicro1900

9. MignotT 2007 The elusive engine in Myxococcus xanthus gliding motility. Cell. Mol. Life Sci 64 2733 2745 doi:10.1007/s00018-007-7176-x

10. SatoKNaitoMYukitakeHHirakawaHShojiM 2010 A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc. Natl Acad Sci U S A 107 276 281 doi:10.1073/pnas.0912010107

11. MaurielloEMFMignotTYangZZusmanDR 2010 Gliding motility revisited: how do the myxobacteria move without flagella? Microbiol. Mol. Biol. Rev 74 229 249 doi:10.1128/MMBR.00043-09

12. MignotTShaevitzJWHartzellPLZusmanDR 2007 Evidence that focal adhesion complexes power bacterial gliding motility. Science 315 853 856 doi:10.1126/science.1137223

13. SunMWartelMCascalesEShaevitzJWMignotT 2011 Motor-driven intracellular transport powers bacterial gliding motility. Proc. Natl Acad Sci 108 U.S.A 7559 7564 doi:10.1073/pnas.1101101108

14. NanBChenJNeuJCBerryRMOsterG 2011 Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. Proc Natl Acad Sci 108 U.S.A 2498 2503 doi:10.1073/pnas.1018556108

15. MaurielloEMFMouhamarFNanBDucretADaiD 2010 Bacterial motility complexes require the actin-like protein, MreB and the Ras homologue, MglA. EMBO J 29 315 326 doi:10.1038/emboj.2009.356

16. YouderianPBurkeNWhiteDJHartzellPL 2003 Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol. Microbiol 49 555 570

17. YuRKaiserD 2007 Gliding motility and polarized slime secretion. Mol. Microbiol 63 454 467 doi:10.1111/j.1365-2958.2006.05536.x

18. NanBMaurielloEMFSunI-HWongAZusmanDR 2010 A multi-protein complex from Myxococcus xanthus required for bacterial gliding motility. Mol. Microbiol 76 1539 1554 doi:10.1111/j.1365-2958.2010.07184.x

19. YehY-CComolliLRDowningKHShapiroLMcAdamsHH 2010 The caulobacter Tol-Pal complex is essential for outer membrane integrity and the positioning of a polar localization factor. J Bacteriol 192 4847 4858 doi:10.1128/JB.00607-10

20. LloubèsRCascalesEWalburgerABouveretELazdunskiC 2001 The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res. Microbiol 152 523 529

21. BlatchGLLässleM 1999 The tetratricopeptide repeat: a structural motif mediating protein-protein interactions. Bioessays 21 932 939 doi:10.1002/(SICI)1521-1878(199911)21:11<932::AID-BIES5>3.0.CO;2-N

22. HammetAPikeBLMcNeesCJConlanLATenisN 2003 FHA domains as phospho-threonine binding modules in cell signaling. IUBMB Life 55 23 27 doi:10.1080/1521654031000070636

23. BustamanteVHMartínez-FloresIVlamakisHCZusmanDR 2004 Analysis of the Frz signal transduction system of Myxococcus xanthus shows the importance of the conserved C-terminal region of the cytoplasmic chemoreceptor FrzCD in sensing signals. Mol. Microbiol 53 1501 1513 doi:10.1111/j.1365-2958.2004.04221.x

24. MaurielloEMFNanBZusmanDR 2009 AglZ regulates adventurous (A-) motility in Myxococcus xanthus through its interaction with the cytoplasmic receptor, FrzCD. Mol. Microbiol 72 964 977 doi:10.1111/j.1365-2958.2009.06697.x

25. GoemaereELCascalesELloubèsR 2007 Mutational analyses define helix organization and key residues of a bacterial membrane energy-transducing complex. J. Mol. Biol 366 1424 1436 doi:10.1016/j.jmb.2006.12.020

26. KarimovaGPidouxJUllmannALadantD 1998 A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci 95 U.S.A 5752 5756

27. KriegNRLudwigWWhitmanWBHedlung BP PasterBJ 2011 Bergey's Manual of Systematic Bacteriology. Dans 948

28. NudlemanEWallDKaiserD 2005 Cell-to-cell transfer of bacterial outer membrane lipoproteins. Science 309 125 127 doi:10.1126/science.1112440

29. LambertCFentonAKHobleyLSockettRE 2011 Predatory bdellovibrio bacteria use gliding motility to scout for prey on surfaces. J Bacteriol 193 3139 3141 doi:10.1128/JB.00224-11

30. GoldmanBSNiermanWCKaiserDSlaterSCDurkinAS 2006 Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci 103 U.S.A 15200 15205 doi:10.1073/pnas.0607335103

31. SémonMWolfeKH 2007 Consequences of genome duplication. Curr. Opin. Genet. Dev 17 505 512 doi:10.1016/j.gde.2007.09.007

32. Van de PeerYMaereSMeyerA 2009 The evolutionary significance of ancient genome duplications. Nat. Rev. Genet 10 725 732 doi:10.1038/nrg2600

33. MüllerF-DTreuner-LangeAHeiderJHuntleySMHiggsPI 2010 Global transcriptome analysis of spore formation in Myxococcus xanthus reveals a locus necessary for cell differentiation. BMC Genomics 11 264 doi:10.1186/1471-2164-11-264

34. ZhangYFrancoMDucretAMignotT 2010 A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol 8 e1000430 doi:10.1371/journal.pbio.1000430

35. BulyhaISchmidtCLenzPJakovljevicVHöneA 2009 Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol. Microbiol 74 691 706 doi:10.1111/j.1365-2958.2009.06891.x

36. MignotTMerlieJPJrZusmanDR 2005 Regulated pole-to-pole oscillations of a bacterial gliding motility protein. Science 310 855 857 doi:10.1126/science.1119052

37. ViarreVCascalesEBallGMichelGPFFillouxA 2009 HxcQ liposecretin is self-piloted to the outer membrane by its N-terminal lipid anchor. J. Biol. Chem 284 33815 33823 doi:10.1074/jbc.M109.065938

38. KahntJAguiluzKKochJTreuner-LangeAKonovalovaA 2010 Profiling the outer membrane proteome during growth and development of the social bacterium Myxococcus xanthus by selective biotinylation and analyses of outer membrane vesicles. J Proteome Res 9 5197 5208 doi:10.1021/pr1004983

39. DucretAMaisonneuveENotareschiPGrossiAMignotT 2009 A microscope automated fluidic system to study bacterial processes in real time. PLoS ONE 4 e7282 doi:10.1371/journal.pone.0007282

40. FinnRDMistryJTateJCoggillPHegerA 2010 The Pfam protein families database. Nucleic Acids Res 38 D211 222 doi:10.1093/nar/gkp985

41. BendtsenJDNielsenHvon HeijneGBrunakS 2004 Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol 340 783 795 doi:10.1016/j.jmb.2004.05.028

42. KroghALarssonBvon HeijneGSonnhammerEL 2001 Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305 567 580 doi:10.1006/jmbi.2000.4315

43. AltschulSFMaddenTLSchäfferAAZhangJZhangZ 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25 3389 3402

44. LarkinMABlackshieldsGBrownNPChennaRMcGettiganPA 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948 doi:10.1093/bioinformatics/btm404

45. PhilippeH 1993 MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res 21 5264 5272

46. BrownJRDouadyCJItaliaMJMarshallWEStanhopeMJ 2001 Universal trees based on large combined protein sequence data sets. Nat. Genet 28 281 285 doi:10.1038/90129

47. BrochierCBaptesteEMoreiraDPhilippeH 2002 Eubacterial phylogeny based on translational apparatus proteins. Trends Genet 18 1 5

48. DelsucFBrinkmannHPhilippeH 2005 Phylogenomics and the reconstruction of the tree of life. Nat. Rev. Genet 6 361 375 doi:10.1038/nrg1603

49. GuindonSGascuelO 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol 52 696 704

50. JobbGvon HaeselerAStrimmerK 2004 TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol. Biol 4 18 doi:10.1186/1471-2148-4-18

51. HuelsenbeckJPRonquistF 2001 MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17 754 755